In 1926 Kangaroo Point was recommended by the Brisbane City Council's Cross River Commission.[3] Subsequently the bridge was constructed as a public works program during the Great Depression. The cost was to be no more than ₤1.6 million.[4]

The Queensland Government appointed John Bradfield on 15 December 1933 as consulting engineer to the Bureau of Industry who were in charge of the construction of the bridge. In June 1934 Bradfield's recommendation of a steel cantilever bridge was approved. The design for the bridge was based heavily on that of the Jacques Cartier Bridge in Montreal, completed in 1930.[3] On 30 April 1935 a consortium of two Queensland companies, Evans Deakin and Hornibrook Constructions, won the tender with a bid of ₤1,150,000.[5][6]

Construction on the bridge began on 24 May 1935,[5] with the first sod being turned by the then Premier of Queensland, William Forgan Smith. Components for the bridge were fabricated in a purpose-built factory at Rocklea. Work sometimes continued 24 hours per day.[4] The bridge has only one pier on the northern bank but two piers on the lower southern bank, one to bear the weight (the main pier) and, further to the south, one to prevent the bridge from twisting (the anchor pier). There was no need for an anchor pier on the northern bank as the bridge was anchored into schist cliff face. The major challenge in constructing the bridge was the southern foundations that went 40 metres below ground level. It was not possible to excavate to that level as water from the level would rapidly seep in. So a pneumatic caisson technique had to be used. As men were working under pressures of up to 4 times normal air pressure, a decompression period of almost 2 hours was needed at the end of each shift to avoid the bends. An on-site air lock hospital successfully treated the 65 cases of the bends that occurred.[6] On 28 October 1939 the gap between the two sides was closed.[5] A concrete decking was then laid, covered by a Trinidad pitch topping. The bridge was painted and sodium lighting was installed. The bridge approaches were also prepared.[6]

The bridge carries an average of 97,000 vehicles each day.[8] The Story Bridge carries three lanes of traffic in either direction as well as a shared pedestrian and cycle way flanking each side. The road on the bridge is called the Bradfield Highway. It is not to be confused with the Bradfield Highway that spans the Sydney Harbour Bridge.

Initially a toll of sixpence (5 cents) was charged to use the bridge,[4] with toll booths constructed at the southern end of the Bradfield Highway. The toll was removed in 1947.[9] Between 1952 and 1969 trolley-buses operated by the Brisbane City Council used the bridge.

Following completion of the bridge, an expressway was constructed on the southern side of the bridge (opened 18 May 1970),[10] and a tunnel/loop was constructed at Kemp Place on the northern side (completed 10 July 1972).[11]

The Story Bridge features prominently in the annual Riverfire display and is illuminated at night. In 1990 road traffic was halted so pedestrians could celebrate the 50th anniversary of the bridge's construction.[4] The bridge was again closed to road traffic on 5 July 2015 to celebrate the 75th anniversary. The celebration attracted almost 75,000 visitors to the bridge who enjoyed food, drink and entertainment as they walked across lanes usually reserved for vehicles.[14]

Bridge climbs began in 2005 and have become a popular tourist attraction.

Similar to many large bridges such as the Golden Gate Bridge in San Francisco, Brisbane's Story Bridge has become notorious as a suicide hotspot.[15] Following two high-profile murder-suicides from the bridge in 2011 and 2012, Brisbane Lord Mayor Graham Quirk announced plans to install free telephones linked to suicide prevention hotlines.[15] On 6 February 2013, Lord Mayor Quirk announced plans to install a three-metre-high safety barrier. Overall the plan cost about $8.4 million and was completed in December 2015.[16]